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1. SAR11 bacteria have a high affinity and multifunctional glycine betaine transporter

   https://doi.org/10.1111/1462-2920.14649  

   Noell, Stephen E. ; Giovannoni, Stephen J. ( May 2019 , Environmental Microbiology)

   Marine bacterioplankton face stiff competition for limited nutrient resources. SAR11, a ubiquitous clade of very small and highly abundantAlphaproteobacteria, are known to devote much of their energy to synthesizing ATP‐binding cassette periplasmic proteins that bind substrates. We hypothesized that their small size and relatively large periplasmic space might enable them to outcompete other bacterioplankton for nutrients. Using uptake experiments with¹⁴C‐glycine betaine, we discovered that two strains of SAR11,CandidatusPelagibacter sp. HTCC7211 andCand. P. ubique HTCC1062, have extraordinarily high affinity for glycine betaine (GBT), with half‐saturation (K_s) values around 1 nM and specific affinity values between 8 and 14 L mg cell⁻¹ h⁻¹. Competitive inhibition studies indicated that the GBT transporters in these strains are multifunctional, transporting multiple substrates in addition to GBT. Both strains could use most of the transported compounds for metabolism and ATP production. Our findings indicate thatPelagibactercells are primarily responsible for the high affinity and multifunctional GBT uptake systems observed in seawater. Maximization of whole‐cell affinities may enable these organisms to compete effectively for nutrients during periods when the gross transport capacity of the heterotrophic plankton community exceeds the supply, depressing ambient concentrations.

    

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2. SAR11 Cells Rely on Enzyme Multifunctionality To Metabolize a Range of Polyamine Compounds

   https://doi.org/10.1128/mBio.01091-21  

   Noell, Stephen E. ; Barrell, Gregory E. ; Suffridge, Christopher ; Morré, Jeff ; Gable, Kevin P. ; Graff, Jason R. ; VerWey, Brian J. ; Hellweger, Ferdi L. ; Giovannoni, Stephen J. ( August 2021 , mBio)

   Dubilier, Nicole (Ed.)

   ABSTRACT In the ocean surface layer and cell culture, the polyamine transport protein PotD of SAR11 bacteria is often one of the most abundant proteins detected. Polyamines are organic cations at seawater pH produced by all living organisms and are thought to be an important component of dissolved organic matter (DOM) produced in planktonic ecosystems. We hypothesized that SAR11 cells uptake and metabolize multiple polyamines and use them as sources of carbon and nitrogen. Metabolic footprinting and fingerprinting were used to measure the uptake of five polyamine compounds (putrescine, cadaverine, agmatine, norspermidine, and spermidine) in two SAR11 strains that represent the majority of SAR11 cells in the surface ocean environment, “ Candidatus Pelagibacter” strain HTCC7211 and “ Candidatus Pelagibacter ubique” strain HTCC1062. Both strains took up all five polyamines and concentrated them to micromolar or millimolar intracellular concentrations. Both strains could use most of the polyamines to meet their nitrogen requirements, but polyamines did not fully substitute for their requirements of glycine (or related compounds) or pyruvate (or related compounds). Our data suggest that potABCD transports all five polyamines and that spermidine synthase, speE, is reversible, catalyzing the breakdown of spermidine and norspermidine, in addition to its usual biosynthetic role. These findings provide support for the hypothesis that enzyme multifunctionality enables streamlined cells in planktonic ecosystems to increase the range of DOM compounds they metabolize. IMPORTANCE Genome streamlining in SAR11 bacterioplankton has resulted in a small repertoire of genes, yet paradoxically, they consume a substantial fraction of primary production in the oceans. Enzyme multifunctionality, referring to enzymes that are adapted to have broader substrate and catalytic range than canonically defined, is hypothesized to be an adaptation that increases the range of organic compounds metabolized by cells in environments where selection favors genome minimization. We provide experimental support for this hypothesis by demonstrating that SAR11 cells take up and metabolize multiple polyamine compounds and propose that a small set of multifunctional enzymes catalyze this metabolism. We report that polyamine uptake rates can exceed metabolic rates, resulting in both high intracellular concentrations of these nitrogen-rich compounds (in comparison to native polyamine levels) and an increase in cell size. 

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3. Pelagibacter metabolism of diatom‐derived volatile organic compounds imposes an energetic tax on photosynthetic carbon fixation

   https://doi.org/10.1111/1462-2920.14861  

   Moore, Eric R. ; Davie‐Martin, Cleo L. ; Giovannoni, Stephen J. ; Halsey, Kimberly H. ( December 2019 , Environmental Microbiology)

   Volatile organic compounds (VOCs) produced by phytoplankton are molecules with high vapor pressures that can diffuse across cell membranes into the environment, where they become public goods. VOCs likely comprise a significant component of the marine dissolved organic carbon (DOC) pool utilized by microorganisms, but they are often overlooked as growth substrates because their diffusivity imposes analytical challenges. The roles of VOCs in the growth of the photoautotrophic diatomThalassiosira pseudonanaand heterotrophic bacteriumPelagibactersp. HTCC1062 (SAR11) were examined using co‐cultures and proton‐transfer reaction time‐of‐flight mass spectrometry. VOCs at 82 m/zvalues were produced in the cultures, and the concentrations of 9 of thesem/zvalues changed in co‐culture relative to the diatom monoculture. Several of them/zvalues were putatively identified, and their metabolism by HTCC1062 was confirmed by measuring ATP production. Diatom carbon fixation rates in co‐culture with HTCC1062 were 20.3% higher than the diatom monoculture. Removal of VOCs from theT. pseudonanamonoculture using a hydrocarbon trap caused a similar increase in carbon fixation (18.1%). These results show that a wide range of VOCs are cycled in the environment, and the flux of VOCs from phytoplankton to bacterioplankton imposes a large and unexpected tax on phytoplankton photosynthesis.

    

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4. Co-culture and biogeography of Prochlorococcus and SAR11

   https://doi.org/10.1038/s41396-019-0365-4  

   Becker, Jamie W. ; Hogle, Shane L. ; Rosendo, Kali ; Chisholm, Sallie W. ( February 2019 , The ISME Journal)

   Prochlorococcus and SAR11 are among the smallest and most abundant organisms on Earth. With a combined global population of about 2.7 × 1028 cells, they numerically dominate bacterioplankton communities in oligotrophic ocean gyres and yet they have never been grown together in vitro. Here we describe co-cultures of Prochlorococcus and SAR11 isolates representing both high- and low-light adapted clades. We examined: (1) the influence of Prochlorococcus on the growth of SAR11 and vice-versa, (2) whether Prochlorococcus can meet specific nutrient requirements of SAR11, and (3) how co-culture dynamics vary when Prochlorococcus is grown with SAR11 compared with sympatric copiotrophic bacteria. SAR11 grew 15–70% faster in co-culture with Prochlorococcus, while the growth of the latter was unaffected. When Prochlorococcus populations entered stationary phase, this commensal relationship rapidly became amensal, as SAR11 abundances decreased dramatically. In parallel experiments with copiotrophic bacteria; however, the heterotrophic partner increased in abundance as Prochlorococcus densities leveled off. The presence of Prochlorococcus was able to meet SAR11’s central requirement for organic carbon, but not reduced sulfur. Prochlorococcus strain MIT9313, but not MED4, could meet the unique glycine requirement of SAR11, which could be due to the production and release of glycine betaine by MIT9313, as supported by comparative genomic evidence. Our findings also suggest, but do not confirm, that Prochlorococcus MIT9313 may compete with SAR11 for the uptake of 3-dimethylsulfoniopropionate (DMSP). To give our results an ecological context, we assessed the relative contribution of Prochlorococcus and SAR11 genome equivalents to those of identifiable bacteria and archaea in over 800 marine metagenomes. At many locations, more than half of the identifiable genome equivalents in the euphotic zone belonged to Prochlorococcus and SAR11 – highlighting the biogeochemical potential of these two groups.

    

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5. Elemental content and stoichiometry of SAR11 chemoheterotrophic marine bacteria

   https://doi.org/10.1002/lol2.10103  

   White, Angelicque E. ; Giovannoni, Stephen J. ; Zhao, Yanlin ; Vergin, Kevin ; Carlson, Craig A. ( February 2019 , Limnology and Oceanography Letters)

   We measured the carbon, nitrogen, and phosphorus content and production of cultured SAR11 cells in the genusPelagibacter, from members of the 1a.1 and 1a.3 lineages, which are adapted to productive coastal waters and oligotrophic tropical/subtropical environments, respectively. The average growing SAR11 cell contained ~ 6.5 fg C, from which we calculated a global standing stock of 1.4 × 10¹³ g C. Calculations that consider uncertainties in cell turnover rates and growth efficiencies indicate this stock could oxidize 6% to 37% of gross ocean primary production. We also found that SAR11 do not incorporate³H‐thymidine but do incorporate³H‐leucine. We estimate conversion factors of 0.74–1.51 kg C mol⁻¹leu, which are comparable to the low end of published leucine conversion factors for marine chemoheterotrophic bacterioplankton production. The molar ratio of elements C : N : P in growing cells was on average 25 : 6 : 1, significantly less than the mean (~ 50 : 10 : 1) for heterotrophic bacteria, indicating these strains are C and N poor relative to P.

    

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